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Coral Spawning in the Gulf of Oman and Relationship to Latitudinal

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Coral Spawning in the Gulf of Oman and Relationship to Latitudinal OPEN Coral spawning in the Gulf of Oman and SUBJECT AREAS: relationship to latitudinal variation in COMMUNITY ECOLOGY ECOSYSTEM ECOLOGY spawning season in the northwest Indian Received Ocean 8 September 2014 E. J. Howells1, D. Abrego2, G. O. Vaughan1 & J. A. Burt1 Accepted 26 November 2014 1Center for Genomics and Systems Biology, New York University Abu Dhabi, PO Box 129188, Abu Dhabi, United Arab Emirates, Published 2Department of Natural Science and Public Health, Zayed University, PO Box 144534, Abu Dhabi, United Arab Emirates. 15 December 2014 Despite a wealth of information on sexual reproduction in scleractinian corals, there are regional gaps in reproductive records. In the Gulf of the Oman in the Arabian Sea, reproductive timing was assessed Correspondence and in four common species of broadcast spawning corals using field surveys of gamete maturity and requests for materials aquarium observations of spawning activity. The appearance of mature gametes within the same month should be addressed to for Acropora downingi, A. hemprichii, Cyphastrea microphthalma and Platygyra daedalea ($ 75% of E.J.H. (em.howells@ colonies, n 5 848) indicated a synchronous and multi-specific spawning season. Based on gamete gmail.com) disappearance and direct observations, spawning predominantly occurred during April in 2013 (75– 100% of colonies) and May in 2014 (77–94% of colonies). The difference in spawning months between survey years was most likely explained by sea temperature and the timing of lunar cycles during late-stage gametogenesis. These reproductive records are consistent with a latitudinal gradient in peak broadcast spawning activity at reefs in the northwestern Indian Ocean which occurs early in the year at low latitudes (January to March) and progressively later in the year at mid (March to May) and high (June to September) latitudes. exual reproduction in scleractinian corals can occur in a variety of forms but the majority of species (.60%) are simultaneous hermaphrodites that spawn both eggs and sperm into the water column1,2. Broadcast spawning allows cross-fertilization between individuals and development of planktonic larvae allows new S 3,4 coral genotypes to disperse across short and large distances . Recruitment of coral larvae is critical to the persistence and recovery of coral assemblages5,6 and enhances adaptive potential by increasing local genetic variation7–9. Broadcast spawning in most individual corals occurs during one or a few nights per year following an annual cycle of gametogenesis2. Synchronous spawning within populations enhances their reproductive success and proposed environmental cues including sea temperature and lunar phase promote spawning during discrete seasons and nights10. Numerous studies of coral reproductive patterns demonstrate coral spawning around the warmest months of the year, yet the duration of spawning seasons and the extent of synchronicity among species and individuals can vary considerably among locations (see reviews by1,2,9,11). Consequently, localised investi- gations are required to determine precise spawning months and nights in data deficient regions. The aim of our study was to record spawning behaviour in corals from the Gulf of Oman, Arabian Sea, for which there were no previous records. We investigated the seasonal and lunar timing of spawning for 4 locally abundant scleractinian species using a combination of 2 years of field surveys and aquarium observa- tions. Locally, these data provide important baseline information for monitoring the health of coral com- munities in the Gulf of Oman which are periodically impacted by damage from fishing gear and anchors12, cyclones13, outbreaks of predatory crown-of-thorns starfish12, oil pollution14,15 and harmful algal blooms16. More broadly, these data contribute to a growing number of records of coral spawning activity in the northwest Indian Ocean17–22 which allowed us to examine latitudinal patterns in spawning behaviour and their underlying environmental drivers. SCIENTIFIC REPORTS | 4 : 7484 | DOI: 10.1038/srep07484 1 www.nature.com/scientificreports (a) 54°E 56°E 58°E 60°E 62°E (b) I r a n (c) 26°N A r a b i a n / P e r s i a n Survey site G u l f s (d) e t a G u l f o f O m a n r i m E 24°N a b A r O U n i t e d m a n A r a b i a n (e) S e a 100 km Figure 1 | Location of reproductive surveys in the Gulf of Oman (a) for the scleractinian corals Acropora downingi (b), Acropora hemprichii (c), Cyphastrea microphthalma (d), Platygyra daedalea (e). Map created by using Adobe Illustrator CS5. Results the lunar cycle or around the new moon. Between 10 nights after the Sexual reproduction was seasonally synchronous in the scleractinian April full moon and 4 nights before the May full moon in 2014, the corals Acropora downingi, A. hemprichii, Cyphastrea microphthalma percentage of colonies with mature gametes sharply declined from and Platygyra daedalea common to the Gulf of Oman23 (Fig. 1). 81% (n 5 53) to 5% (n 5 58) in A. downingi and from 95% (n 5 41) Mature gametes developed in $ 75% of colonies of each species prior to 33% in A. hemprichii. This reproductive timing is supported by to one of the spring full-moons and disappeared by the following aquarium spawning of A. downingi (n 5 8) which occurred in all month, indicating that spawning had occurred (Fig. 2a). In 2013, the colony fragments on 13 and/or 14 nights after the full moon (i.e. new majority of colonies belonging to each species (75 to 100%) moon) in April 2013. developed mature gametes by the April full moon (25th), whereas in 2014, gamete maturation did not occur in most colonies (77 to Discussion th 94%) until prior to the May full moon (14 ). This inter-annual Patterns of sexual reproduction in corals from the Gulf of Oman variation in spawning timing corresponded with lower monthly demonstrate that coral communities in the northern Arabian Sea average sea temperatures in the lead up to the 2014 spawning, includ- engage in seasonally synchronous spawning events, such as those ing average sea temperature preceding the April full moon that were that have been observed in numerous other tropical and temperate 1.5uC lower in 2014 compared with 2013 (Fig. 2b). reef ecosystems (e.g. refs. 10, 25, 26). The April to May timing of Additional field and aquarium observations of Gulf of Oman cor- spawning in acroprid and merulind corals observed in the Gulf of als demonstrated variation in the lunar phase of spawning among the Oman is consistent with spawning months of corals from these fam- 24 coral species being studied. The merulinids (formerly favids ) C. ilies at latitudes (22–27uN) from nearby regions of the Arabian/ microphthalma and P. daedalea spawned around the full moon, as Persian Gulf17 and the Red Sea20,27. At lower latitude (13uN) in the indicated by the timing of disappearance of mature eggs between 4 southern Arabian Sea, surveys of egg maturity indicate that at least days before and 12 days after the full moon in May 2014 (Table 1). half of the acroporid corals spawn in February and March22 which is The percentage of colonies with mature eggs declined from 88% (n 5 consistent with the peak of spawning activity in acroporid and mer- 25) to 23% (n 5 21) in C. microphthalma and from 56% (n 5 41) to ulinid corals from equatorial reefs in the Indian Ocean18,19. In con- 0% (n 5 42) in P. daedalea. A small proportion (22%) of P. daedalea trast, at higher latitude (30uN), broadcast spawning in most coral colonies had mature gamete bundles 7 days before the full moon in species occurs from June to September (northern Red Sea28). These April. These colonies likely began spawning after the April full moon results combined show a latitudinal gradient in seasonality of peak and may have still been releasing by the next survey 10 days after the broadcast spawning activity in corals from the northwest Indian full moon. Thus, the high proportion of colonies found with mature Ocean with spawning earlier in the year close to the equator and bundles 10 days after the April full moon may reflect colonies that later in the year with increasing northward latitude (r50.75, p were still spawning as well as those colonies with bundles mature ,0.01, Fig. 3). enough to be released after the May full moon. This interpretation is Coral spawning during annual periods of sea temperature rise has supported by an extended spawning window observed in fragments been well documented29. Latitudinal differences in spawning seasons from individual P. daedalea colonies (n 5 10) kept in aquaria in April in the northwest Indian Ocean are likely due to variation in temper- 2013. These colonies released gametes for up to 10 consecutive ature profiles and are consistent with latitudinal trends in coral nights. Spawning occurred from 19:45 to 21:30 (1:00 to 2:45 hours reproduction in the northwest Pacific30. For example, sites closer to after sunset) from 2 nights before the full moon to 9 nights after the the equator (,13uN; sites 10, 12–13 in Fig. 3) reach their annual full moon (when observations ceased), with a spawning peak 3 nights maximum temperatures earlier in the year (March to May) com- after full moon when all colony fragments released gametes. pared with higher latitude sites (.22uN; sites 5–9 in Fig. 3) which In contrast, field surveys of the acroporids A. downingi and A. reach their maximum later in the year (July to August). The delayed hemprichii indicated that the majority of colonies spawned later in spawning peak at the highest latitude and coolest region of the Red
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